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Inter- and Intra- Species Variation in Secondary Metabolites

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Inter- and Intra- Species Variation in Secondary Metabolites INTER- AND INTRA- SPECIES VARIATION IN SECONDARY METABOLITES FROM CARIBBEAN OCTOCORALS OF THE GENUS PSEUDOPTEROGORGIA: ANTIOXIDANT ACTIVITY AND A POTENTIAL ECOLOGICAL ROLE by MAIA STAPLETON MUKHERJEE (Under the direction of William K. Fitt) ABSTRACT Trends of the past century suggest that coral bleaching events may become more frequent and severe as the climate continues to warm, exposing coral reefs to an increasingly hostile environment. The combination of higher than average temperatures (as small as 1°C–2°C) and intense light can lead to mass coral bleaching events, which result in apoptosis and/or the expulsion of the zooxanthellae from the host tissue. The decline of coral reefs is significant, because coral reefs maintain high levels of biodiversity, provide habitats for coastal fisheries, protect shorelines from erosion, and may contain potential pharmacological compounds. A striking difference between Caribbean octocorals and other zooxanthellate cnidarians is their seemingly greater resistance of bleaching. While there have been numerous reports of scleractinian coral bleaching throughout the world’s tropical oceans, there have been far fewer observations of bleaching among octocorals. If the increasing incidence of bleaching events continues, the relative insensitivity of most gorgonians to high temperatures may have important consequences for Caribbean reefs. This research attempts to examine whether secondary metabolites from the genus Pseudopterogorgia act as antioxidants and thus mediate thermal and UV induced oxidative stress and thereby protect the coral-algal symbiosis. Chemical diversity in soft corals may have an adaptive value in mediating ecological interactions in reef environments. Extracts from Pseudopterogorgia sps have differing antioxidant potentials as seen using the FRAP assay. Diterpenes isolated from P elisabethae exhibit antioxidant potential in FRAP and pseudopterosins scavenge superoxide radicals generated in mouse neuronal cells deprived of NGF and prevent apoptosis. Most significantly, pseudopterosins (and especially the aglycone) reduce the loss of quantum photosynthetic yield in zooxanthellae exposed to excess heat and light, and reduced significantly the oxidation of the probe DCFH in the zooxanthellae/ micro-plate based assay. Index Words: Coral bleaching, Photoinhibition, Octocoral, Zooxanthellae, Antioxidant, Pseudopterogorgia, Pseudopterosin, Natural product, FRAP, DCFH-DA, Nerve Growth Factor, Diterpene INTER- AND INTRA- SPECIES VARIATION IN SECONDARY METABOLITES FROM CARIBBEAN OCTOCORALS OF THE GENUS PSEUDOPTEROGORGIA: ANTIOXIDANT ACTIVITY AND A POTENTIAL ECOLOGICAL ROLE by MAIA STAPLETON MUKHERJEE B.A., Michigan State University, 1987 B.A., Michigan State University, 1988 M.A., New York University, 1998 M.S., Florida Atlantic University, 2005 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2008 ©2008 Maia Stapleton Mukherjee All Rights Reserved INTER- AND INTRA- SPECIES VARIATION IN SECONDARY METABOLITES FROM CARIBBEAN OCTOCORALS OF THE GENUS PSEUDOPTEROGORGIA: ANTIOXIDANT ACTIVITY AND A POTENTIAL ECOLOGICAL ROLE by MAIA STAPLETON MUKHERJEE Major Professor: William K. Fitt Committee: James W. Porter James L. Franklin James L. Shelton C. Ronald Carroll Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia December, 2008 DEDICATION For my father and mother; we were but stones; your light made us stars. For Kevin, who reminds me every day that the world is full of wondrous discoveries yet to be made. iv ACKNOWLEDGEMENTS Thanks to my advisor, Dr. William Fitt, and the members of my committee, Dr. Jim Porter, Dr. Jim Franklin, Dr. Jay Shelton and Dr. Ron Carroll for all the support and advice. Thanks to Dr. Gregory Schmidt and Dr. Bill Fitt for allowing me to use cultures of Symbiodinium spp and the PAM Fluorometer. Thanks to Clint Oakley for assisting me with the zooxanthellae based assays. Thanks to Rebecca Kirkland and Jim Franklin for performing the assays with mouse sympathetic neurons. Thanks to Dr. Prasoon Gupta and Dr. Lyndon West for the structural elucidation and characterization of pseudopterosins. Additional thanks to Dr. West his support and for generously allowing me to use the facilities in his lab to conduct my research. Thanks to Dr. Howard Lasker for supporting my field work, for generously sharing his expertise in octocoral biology and ecology, and all his advice and encouragement. Finally a very special thanks to the Mukherjees; mom, dad, Joia, Janam, Che, and Kevin- “If not for you, winter would have no spring, couldn't hear the robin sing, I just wouldn't have a clue, anyway it wouldn't ring true, if not for you.” v TABLE OF CONTENTS ACKNOWLEDGEMENTS……………………………………………………… v LIST OF TABLES………………………………………………………………... viii LIST OF FIGURES………………………………………………………………. x CHAPTER 1 Introduction and Background……………………………………….. 1 1.1-Coral reefs and coral bleaching………………………………….. 1 1.2-Natural products………………………………………………….. 10 1.3-Marine natural products……………………................................. 13 1.4 Reactive oxygen and antioxidants……………………………….. 26 1.5 The antioxidant potential of extracts and compounds from Pseudopterogorgia sps………………………………………………… 32 2 Intra-specific chemical variability of Pseudopterogorgia elisabethae 37 2.1 Caribbean octocorals……………………………………………... 37 2.2 Terpene Biosynthesis……………………………………………... 38 2.3 Terpenes from Pseudopterogorgia spp…………………………... 40 2.4 Pseudopterosins…………………………………………………… 42 2.5 Variability of pseudopterosin content across a geographic gradient................................................................................................... 52 vi 3 Antioxidant potential of extracts and pure compounds from Pseudopterogorgia sps………………………………………………………. 68 3.1 Antioxidants and marine organisms…………………………….. 68 3.2 Ferric reducing antioxidant power (FRAP) assay……………… 70 4 In vivo antioxidant activity of extracts and pure compounds from Pseudopterogorgia…………………………………………………………... 90 4.1 Photosynthesis and oxidative stress……………………………… 90 4.2 Detection of intracellular ROS using 2’,7’- dichlorodihydrofluorescein diacetate………………………………... 92 4.3 Detection of photoinhibition using PAM fluorometry………….. 100 5 A potential pharmacological role for the antioxidants from Pseudopterogorgia sps………………………………………………………. 110 5.1 Oxidative stress and human diseases………………..................... 110 5.2 Oxidative stress and neurodengerative diseases………………... 112 5.3 Pseudopterosins promote survival in NGF deprived mouse sympathetic neurons………………………………………………….. 116 5.4 Pseudopterosins suppress ROS formation in NGF deprived sympathetic neurons………………………………………………….. 118 6 Methods and materials………………………………………………... 123 REFERENCES……………………………………………………………………. 133 APPENDICES…………………………………………………………………….. 163 vii LIST OF TABLES Table 1. Comparison of pseudopterosin A-D and kallolide A Acetate content from P. elisabethae and P. bipinnata expressed as % organic extract... 49 Table 2. Comparison specific activities of pseudopterosin and Kallolide A acetate from larvae treated with antibiotics and antimycotics and those untreated. Average of n = 3 experiments ± st. dev…………………… 51 Table 3. Distribution of pseudopterosins. Sites are grouped by chemotype. Values reported as %w/w of the 75% fraction of the crude extract…………………………………………………………………. 63 Table 4. FRAP assay of the intermediate polarity (75%) fraction of seven species of Pseudopterogorgia. Values given are µM of Trolox / µg extract, n=4 ± standard deviation. Different letters indicate significantly different means (P <0.01), Tukey’s HSD……………….. 76 Table 5. FRAP assay of pure pseudopterosins and related molecules isolated from Pseudopterogorgia elisabethae Values given are µM of Trolox / µg extract, n=4 ± standard deviation. Different letters indicate significantly different means (P <0.01), Tukey’s HSD……………….. 82 Table 6. DCFH-DA assay of the intermediate polarity (75%) fraction of seven species of Pseudopterogorgia. Values given are % reduction in DCF fluorescence versus MeOH control, n=4 ± standard deviation. Different letters indicate significantly different means (P <0.01), Tukey’s HSD………………………………………………………….. 96 Table 7. DCFH-DA assay of pure pseudopterosins and related molecules isolated from Pseudopterogorgia elisabethae, given as percent fluorescence inhibition versus control cells (MeOH only) n=4 ± standard deviation. Different letters indicate significantly different means (P <0.01), Tukey’s HSD……………………….......................... 98 Table 8. Pairwise comparison of treatments; Tukey’s HSD, p<0.05…………... 106 Table A1. GPS coordinates of Pseudopterogorgia sps. collection sites…………. 163 Table A2. One-way analysis of variance for FRAP assay of 75% fractions from seven species of the genus Pseudopterogorgia shows that means are significantly different amongst the treatments. (Graphpad Prism)……. 163 viii Table A3. One-way analysis of variance for FRAP assay of 15 pseudopterosins isolated from Pseudopterogorgia elisabethae shows that means are significantly different amongst the treatments. The water soluble vitamin E analog Trolox serves as the positive control. (Graphpad Prism)………………………………………………………………….. 164 Table A4. One-way analysis of variance for DCFH-DA - zooxanthellae assay of 75% fractions from seven species of the genus Pseudopterogorgia shows that means are significantly different amongst the treatments. Cells with no treatment and cells
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